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Effect of progressive resistance training on persistent pain after axillary dissection in breast cancer: a randomized controlled trial

  • Gunn AmmitzbøllEmail author
  • Kenneth Geving Andersen
  • Pernille Envold Bidstrup
  • Christoffer Johansen
  • Charlotte Lanng
  • Niels Kroman
  • Bo Zerahn
  • Ole Hyldegaard
  • Elisabeth Wreford Andersen
  • Susanne Oksbjerg Dalton
Clinical trial

Abstract

Purpose

Persistent pain is a known challenge among breast cancer survivors. In secondary analyses of a randomized controlled trial, we examined the effect of progressive resistance training on persistent pain in the post-operative year in women treated for breast cancer with axillary lymph node dissection.

Methods

We randomized 158 women after BC surgery with Axillary Lymph Node Dissection (ALND) (1:1) to usual care or a 1-year, supervised and self-administered, progressive resistance training intervention initiated 3 weeks after surgery. A questionnaire at baseline, 20 weeks and 12 months assessed the intensity and frequency of pain, neuropathic pain and influence of pain on aspects of daily life. We analysed the effect using linear mixed models and multinomial logistic regression models for repeated measures.

Results

A high percentage of participants experienced baseline pain (85% and 83% in the control and intervention groups respectively) and by the 12 month assessment these numbers were more than halved. A high proportion of participants also experienced neuropathic pain (88% and 89% in control and intervention group respectively), a finding that was stable throughout the study period. The effect on intensity of pain indicators favoured the exercise group, although most estimates did not reach statistical significance, with differences being small.

Conclusion

For women who had BC surgery with ALND, our progressive resistance training intervention conferred no benefit over usual care in reducing pain. Importantly, it did not increase the risk of pain both in the short and long term rehabilitative phase.

Keywords

Oncology Breast cancer Axillary lymph node dissection Pain Resistance training 

Notes

Author contributions

GA participated in designing and executing the experiment, and in writing the manuscript. KGA was involved in designing the measurement tools, planning the analyses and in the writing of the manuscript. PEB was involved in planning the analyses and in the writing of the manuscript. CJ, NK, BZ, OH and SOD participated in designing the experiment and in writing the manuscript. CL participated in planning and execution of the study and in writing the manuscript. EWA was involved in planning and performing the statistical analyses and in writing the manuscript.

Funding

This work was supported by The Danish Cancer Society, (Grant Number R96-A6604-14-S22) and Tryg Fonden (Grant Number ID 112305).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

The study was approved by the ethical committee in the ethical approval (H-15002714), and all procedures were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

All participants gave informed consent to participate before any study related activities were performed.

Supplementary material

10549_2019_5461_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 kb)
10549_2019_5461_MOESM2_ESM.docx (28 kb)
Supplementary material 2 (DOCX 28 kb)

References

  1. 1.
    Mejdahl MK, Andersen KG, Gartner R, Kroman N, Kehlet H (2013) Persistent pain and sensory disturbances after treatment for breast cancer: six year nationwide follow-up study. BMJ 346:f1865CrossRefGoogle Scholar
  2. 2.
    Meretoja TJ, Leidenius MHK, Tasmuth T, Sipila R, Kalso E (2014) Pain at 12 months after surgery for breast cancer. JAMA 311(1):90–92CrossRefGoogle Scholar
  3. 3.
    Andersen KG, Duriaud HM, Jensen HE, Kroman N, Kehlet H (2015) Predictive factors for the development of persistent pain after breast cancer surgery. Pain 156(12):2413–2422CrossRefGoogle Scholar
  4. 4.
    Meretoja TJ, Andersen KG, Bruce J, Haasio L, Sipila R, Scott NW et al (2017) Clinical prediction model and tool for assessing risk of persistent pain after breast cancer surgery. J Clin Oncol 35(15):1660–1667CrossRefGoogle Scholar
  5. 5.
    Aaronson NK, Ahmedzai S, Bergman B, Bullinger M, Cull A, Duez NJ et al (1993) The European organization for research and treatment of cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst 85(5):365–376CrossRefGoogle Scholar
  6. 6.
    Andersen KG, Jensen MB, Tvedskov TF, Kehlet H, Gartner R, Kroman N (2013) Persistent pain, sensory disturbances and functional impairment after immediate or delayed axillary lymph node dissection. Eur J Surg Oncol 39(1):31–35CrossRefGoogle Scholar
  7. 7.
    Leysen L, Beckwee D, Nijs J, Pas R, Bilterys T, Vermeir S et al (2017) Risk factors of pain in breast cancer survivors: a systematic review and meta-analysis. Support Care Cancer 25(12):3607–3643CrossRefGoogle Scholar
  8. 8.
    Andersen KG, Kehlet H (2011) Persistent pain after breast cancer treatment: a critical review of risk factors and strategies for prevention. J Pain 12(7):725–746CrossRefGoogle Scholar
  9. 9.
    Miaskowski C, Cooper B, Paul SM, West C, Langford D, Levine JD et al (2012) Identification of patient subgroups and risk factors for persistent breast pain following breast cancer surgery. J Pain 13(12):1172–1187CrossRefGoogle Scholar
  10. 10.
    Miaskowski C, Paul SM, Cooper B, West C, Levine JD, Elboim C et al (2014) Identification of patient subgroups and risk factors for persistent arm/shoulder pain following breast cancer surgery. Eur J Oncol Nurs 18(3):242–253CrossRefGoogle Scholar
  11. 11.
    Bruce J, Thornton AJ, Powell R, Johnston M, Wells M, Heys SD et al (2014) Psychological, surgical, and sociodemographic predictors of pain outcomes after breast cancer surgery: a population-based cohort study. Pain 155(2):232–243CrossRefGoogle Scholar
  12. 12.
    Mejdahl MK, Mertz BG, Bidstrup PE, Andersen KG (2015) Preoperative distress predicts persistent pain after breast cancer treatment: a prospective cohort study. J Natl Compr Cancer Netw 13(8):995–1003 (quiz) Google Scholar
  13. 13.
    Goldfarb A (2013) Exercise and endogenous opiates. Endocrinology of physical activity and sport, 2nd edn. Humana Press, Totowa, pp 21–36CrossRefGoogle Scholar
  14. 14.
    Kami K, Tajima F, Senba E (2017) Exercise-induced hypoalgesia: potential mechanisms in animal models of neuropathic pain. Anat Sci Int 92(1):79–90CrossRefGoogle Scholar
  15. 15.
    Naugle KM, Fillingim RB, Riley JL 3rd (2012) A meta-analytic review of the hypoalgesic effects of exercise. J Pain 13(12):1139–1150CrossRefGoogle Scholar
  16. 16.
    Kroll HR (2015) Exercise therapy for chronic pain. Phys Med Rehabil Clin N Am 26(2):263–281CrossRefGoogle Scholar
  17. 17.
    Haff G, Triplett N (2015) Essentials of strength training and conditioning, 6th–7th edn. Human Kinetics, Champaign, pp 115–135Google Scholar
  18. 18.
    Furmaniak AC, Menig M, Markes MH (2016) Exercise for women receiving adjuvant therapy for breast cancer. Cochrane Database Syst Rev 9:Cd005001Google Scholar
  19. 19.
    Lahart IM, Metsios GS, Nevill AM, Carmichael AR (2018) Physical activity for women with breast cancer after adjuvant therapy. Cochrane Database Syst Rev 1:Cd011292Google Scholar
  20. 20.
    McNeely ML, Campbell K, Ospina M, Rowe BH, Dabbs K, Klassen TP et al (2010) Exercise interventions for upper-limb dysfunction due to breast cancer treatment. Cochrane Database Syst Rev 6:Cd005211Google Scholar
  21. 21.
    Cheema BS, Kilbreath SL, Fahey PP, Delaney GP, Atlantis E (2014) Safety and efficacy of progressive resistance training in breast cancer: a systematic review and meta-analysis. Breast Cancer Res Treat 148(2):249–268CrossRefGoogle Scholar
  22. 22.
    Hwang JH, Chang HJ, Shim YH, Park WH, Park W, Huh SJ et al (2008) Effects of supervised exercise therapy in patients receiving radiotherapy for breast cancer. Yonsei Med J 49(3):443–450CrossRefGoogle Scholar
  23. 23.
    Cormie P, Pumpa K, Galvao DA, Turner E, Spry N, Saunders C et al (2013) Is it safe and efficacious for women with lymphedema secondary to breast cancer to lift heavy weights during exercise: a randomised controlled trial. J Cancer Surviv 7(3):413–424CrossRefGoogle Scholar
  24. 24.
    Sundheddstyrelsen. National Clinical Guidelines concerning complications following surgery for early breast cancer- prevention, treatment and rehabilitation of impairments in shoulder and arm and arm lymphedema in adults who have undergone surgery for early breast cancer Copenhagen: Sundhedsstyrelsen; 2016Google Scholar
  25. 25.
    Kirkham AA, Bland KA, Sayyari S, Campbell KL, Davis MK (2016) Clinically relevant physical benefits of exercise interventions in breast cancer survivors. Curr Oncol Rep 18(2):12CrossRefGoogle Scholar
  26. 26.
    Danish Breast Cancer Cooperative Group [internet]. Copenhagen: Danish Breast Cancer Cooperative Group; [Nationwide clincial database]. http://www.dbcg.dk/
  27. 27.
    Jensen MB, Laenkholm AV, Offersen BV, Christiansen P, Kroman N, Mouridsen HT et al (2018) The clinical database and implementation of treatment guidelines by the Danish Breast Cancer Cooperative Group in 2007–2016. Acta Oncol 57(1):13–18CrossRefGoogle Scholar
  28. 28.
    Ammitzboll G, Johansen C, Lanng C, Andersen EW, Kroman N, Zerahn B et al (2019) Progressive resistance training to prevent arm lymphedema in the first year after breast cancer surgery: results of a randomized controlled trial. Cancer 125(10):1683–1692CrossRefGoogle Scholar
  29. 29.
    Ammitzbøll G, Lanng C, Kroman N, Zerahn B, Hyldegaard O, Kaae Andersen K et al (2017) Progressive strength training to prevent LYmphoedema in the first year after breast CAncer—the LYCA feasibility study. Acta Oncol 56(2):360–366CrossRefGoogle Scholar
  30. 30.
    Heyward V, Gibson A (2014) Assessing muscular fitness. In: Huls S (ed) Advanced fitness assessment and exercise prescription, 7th edn. Human Kinetics, Champaign, pp 153–180Google Scholar
  31. 31.
    Gartner R, Jensen MB, Nielsen J, Ewertz M, Kroman N, Kehlet H (2009) Prevalence of and factors associated with persistent pain following breast cancer surgery. JAMA 302(18):1985–1992CrossRefGoogle Scholar
  32. 32.
    Mejdahl MK, Christensen KB, Andersen KG (2019) Development and validation of a screening tool for surgery-specific neuropathic pain scale for postsurgical patients. Pain Phys 22:81–90Google Scholar
  33. 33.
    Torres Lacomba M, Yuste Sanchez MJ, Zapico Goni A, Prieto Merino D, Mayoral del Moral O, Cerezo Tellez E et al (2010) Effectiveness of early physiotherapy to prevent lymphoedema after surgery for breast cancer: randomised, single blinded, clinical trial. BMJ 340:b5396CrossRefGoogle Scholar
  34. 34.
    Box RC, Reul-Hirche HM, Bullock-Saxton JE, Furnival CM (2002) Physiotherapy after breast cancer surgery: results of a randomised controlled study to minimise lymphoedema. Breast Cancer Res Treat 75(1):51–64CrossRefGoogle Scholar
  35. 35.
    Johansson K, Branje E (2010) Arm lymphoedema in a cohort of breast cancer survivors 10 years after diagnosis. Acta Oncol 49(2):166–173CrossRefGoogle Scholar
  36. 36.
    Ammitzboll G, Johansen C, Lanng C, Andersen EW, Kroman N, Zerahn B et al (2019) Progressive resistance training to prevent arm lymphedema in the first year after breast cancer surgery: results of a randomized controlled trial. Cancer 125:1683–1692CrossRefGoogle Scholar
  37. 37.
    Kootstra JJ, Dijkstra PU, Rietman H, de Vries J, Baas P, Geertzen JH et al (2013) A longitudinal study of shoulder and arm morbidity in breast cancer survivors 7 years after sentinel lymph node biopsy or axillary lymph node dissection. Breast Cancer Res Treat 139(1):125–134CrossRefGoogle Scholar
  38. 38.
    Akoochakian M, Davari HA, Alizadeh MH, Rahnama N (2017) Evaluation of shoulder girdle strength more than 12 month after modified radical mastectomy and axillary nodes dissection. J Res Med Sci 22:81CrossRefGoogle Scholar
  39. 39.
    Hidding JT, Beurskens CH, van der Wees PJ, van Laarhoven HW, Nijhuis-van der Sanden MW (2014) Treatment related impairments in arm and shoulder in patients with breast cancer: a systematic review. PLoS ONE 9(5):e96748CrossRefGoogle Scholar
  40. 40.
    Gerbershagen HJ, Rothaug J, Kalkman CJ, Meissner W (2011) Determination of moderate-to-severe postoperative pain on the numeric rating scale: a cut-off point analysis applying four different methods. Br J Anaesth 107(4):619–626CrossRefGoogle Scholar
  41. 41.
    Sagen A, Karesen R, Risberg MA (2009) Physical activity for the affected limb and arm lymphedema after breast cancer surgery. A prospective, randomized controlled trial with two years follow-up. Acta Oncol 48(8):1102–1110CrossRefGoogle Scholar
  42. 42.
    Reis AD, Pereira P, Diniz RR, de Castro Filha JGL, Dos Santos AM, Ramallo BT et al (2018) Effect of exercise on pain and functional capacity in breast cancer patients. Health Qual Life Outcomes 16(1):58CrossRefGoogle Scholar
  43. 43.
    Kleckner IR, Kamen C, Gewandter JS, Mohile NA, Heckler CE, Culakova E et al (2018) Effects of exercise during chemotherapy on chemotherapy-induced peripheral neuropathy: a multicenter, randomized controlled trial. Support Care Cancer 26(4):1019–1028CrossRefGoogle Scholar
  44. 44.
    de Jesus Leite MAF, Puga GM, Arantes FJ, Oliveira CJF, Cunha LM, Bortolini MJS et al (2018) Effects of combined and resistance training on the inflammatory profile in breast cancer survivors: a systematic review. Complement Ther Med 36:73–81CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Gunn Ammitzbøll
    • 1
    • 2
    Email author
  • Kenneth Geving Andersen
    • 3
    • 4
  • Pernille Envold Bidstrup
    • 5
  • Christoffer Johansen
    • 1
    • 6
  • Charlotte Lanng
    • 7
  • Niels Kroman
    • 7
    • 8
  • Bo Zerahn
    • 9
  • Ole Hyldegaard
    • 10
    • 11
  • Elisabeth Wreford Andersen
    • 12
  • Susanne Oksbjerg Dalton
    • 1
    • 2
  1. 1.Survivorship and Inequality in CancerDanish Cancer Society Research CenterCopenhagenDenmark
  2. 2.Department of Clinical Oncology and Palliative CareZealand University HospitalNæstvedDenmark
  3. 3.Department of Anaesthesiology and Intensive CareZealand University HospitalKøgeDenmark
  4. 4.Section for Surgical PathophysiologyRigshospitaletCopenhagenDenmark
  5. 5.Psychosocial Aspects in CancerDanish Cancer Society Research CenterCopenhagenDenmark
  6. 6.CASTLE Late Effects Unit, Department of OncologyCopenhagen University Hospital RigshospitaletCopenhagenDenmark
  7. 7.Department of Breast SurgeryCopenhagen University Hospital Herlev/RigshospitaletCopenhagenDenmark
  8. 8.Danish Cancer SocietyCopenhagenDenmark
  9. 9.Department of Clinical Physiology and Nuclear MedicineCopenhagen University Hospital HerlevCopenhagenDenmark
  10. 10.Section for Hyperbaric Oxygen Treatment, Department for Anaesthetics and OperationsCopenhagen University Hospital RigshospitaletCopenhagenDenmark
  11. 11.Institute of Clinical Medicine, University of CopenhagenCopenhagenDenmark
  12. 12.Unit of Statistics and PharmacoepidemiologyDanish Cancer Society Research CenterCopenhagenDenmark

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